Energetics of metamorphosis in Drosophila melanogaster

We measured the energetic cost of metamorphosis in the fruitfly, Drosophila melanogaster. Metabolic rates decreased rapidly in the first 24 h and remained low until shortly before eclosion, when the rates increased rapidly, thus creating a U-shaped metabolic curve. The primary fuel used during metamorphosis was lipid, which accounted for >80% of total metabolism. The total energy consumed during metamorphosis was lowest at 25 °C, compared to 18 and 29 °C, due to differences in metabolic rates and the length of pupal development. Temperature differentially affected metabolic rates during different stages of metamorphosis. Prepupal and late pupal stages exhibited typical increases in metabolic rate at high temperatures, whereas metabolic rates were independent of temperature during the first 2/3 of pupal development.We tested two hypotheses for the underlying cause of the U-shaped metabolic curve. The first hypothesis was that pupae become oxygen restricted as a result of remodeling of the larval tracheal system. We tested this hypothesis by exposing pupae to hypoxic and hyperoxic atmospheres, and by measuring lactic acid production during normoxic development. No evidence for oxygen limitation was observed. We also tested the hypothesis that the U-shaped metabolic curve follows changes in metabolically active tissue, such that the early decrease in metabolic rates reflects the histolysis of larval tissues, and the later increase in metabolic rates is associated with organogenesis and terminal differentiation of adult tissues. We assayed the activity of a mitochondrial indicator enzyme, citrate synthase, and correlated it with tissue-specific developmental events during metamorphosis. Citrate synthase activity exhibited a U-shaped curve, suggesting that the pattern of metabolic activity is related to changes in the amount of potentially active aerobic tissue.

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► Metabolic rates of Drosophila exhibit a U-shaped pattern during metamorphosis.
► The energetic cost of metamorphosis increases at low or high temperatures.
► Pupae do not undergo significant anaerobic metabolism.
► Citrate synthase activity also exhibited a U-shaped curve.
► The U-shaped curve occurs as larval tissue is lost and replaced by adult tissue.